The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex

Abstract

Behavioral and neurophysiological studies suggest that skill learning can be mediated by discrete, experience-driven changes within specific neural representations subserving the performance of the trained task. We have shown that a few minutes of daily practice on a sequential finger opposition task induced large, incremental performance gains over a few weeks of training. These gains did not generalize to the contralateral hand nor to a matched sequence of identical component movements, suggesting that a lateralized representation of the learned sequence of movements evolved through practice. This interpretation was supported by functional MRI data showing that a more extensive representation of the trained sequence emerged in primary motor cortex after 3 weeks of training. The imaging data, however, also indicated important changes occurring in primary motor cortex during the initial scanning sessions, which we proposed may reflect the setting up of a task-specific motor processing routine. Here we provide behavioral and functional MRI data on experience-dependent changes induced by a limited amount of repetitions within the first imaging session. We show that this limited training experience can be sufficient to trigger performance gains that require time to become evident. We propose that skilled motor performance is acquired in several stages: "fast" learning, an initial, within-session improvement phase, followed by a period of consolidation of several hours duration, and then "slow" learning, consisting of delayed, incremental gains in performance emerging after continued practice. This time course may reflect basic mechanisms of neuronal plasticity in the adult brain that subserve the acquisition and retention of many different skills.

Figures

Figure 1

The effects of long-term practice on sequence performance. (A) The two sequences of finger-to-thumb opposition movements used in our study (6). In sequence A the order of finger movements was 4,1,3,2,4 (numbering the fingers from index to little), and in sequence B the order was 4,2,3,1,4 as indicated by the arrows (matched, mirror-reversed sequences). Practice consisted of tapping the designated training sequence as fast and accurately as possible for 10–20 min a day, a few minutes at a time separated by half-minute rests. (B) Learning curves, trained sequence. Each curve (symbol) depicts the performance of a single subject as a function of time. Pre-training (time point 0), day 3 and 10 of training, and performance on the day of the subsequent weekly imaging sessions is shown for 10 subjects. The number of complete sequences performed in a 30-sec test interval (rate) increased from 17.4 ± 3.9 to 38.4 ± 5.8 (mean, SD; week 0 and 5 weeks of training, respectively; paired t test, P < 0.001). Accuracy improved, too, with the number of sequences that contained errors decreasing from a mean of 2.4 ± 0.9 to 0.5 ± 0.5 (paired t test, P < 0.001). (C) No significant improvement for the control sequence (performance rate 18.1 ± 3.7 to 19.4 ± 4.2; 0 and 5 weeks of training, respectively; paired t test, not significant). (D) There was little or no transfer of the learning effect to the contralateral (dominant) hand. Trained (T) vs. control (C) sequence performance rates, at week 5, were 22.3 ± 2.9 and 19.8 ± 4.0, respectively (paired t test, P = 0.097).

Figure 2

Differential evoked responses in M1 to the trained vs. the untrained (control) sequence. Training and performance during scanning done with the left (nondominant) hand. (a and b) Emergence of differential activation after 3 weeks of daily practice on the designated training sequence. (c and d) Maintained differential activation 8 weeks later with no additional training in the interval. Sagital sections through the right hemisphere centered ≈35 mm from midline are shown: right, anterior; top, dorsal aspect of the brain. The activity-dependent blood-oxygenation-level-dependent signals evoked by the trained sequence are shown in a and c. Those evoked by the untrained sequence are shown in b and d. Z-score values are indicated by the pseudo-color scale. A surface coil was used, which had the advantage of providing enhanced signal-to-noise ratios, but at the cost of limiting the data to M1 and surrounding areas contralateral to the performing hand. Imaging parameters are given in ref. . The comparison is always to the control sequence, performed within the same set. No direct comparison is possible because of different shims and a somewhat different placing of the subject in the magnet and of the surface coil on the subject’s head. The area of evoked signal in M1 was consistently larger in extent for the trained as compared with the untrained sequence by 3 weeks of training and remained so 8 weeks later.

Figure 3

Cortical and behavioral effects of short-term practice. (A) Cortical effects. The ordering effects during the initial imaging session: The mean difference in the extent of the evoked signal calculated as the difference in the number of pixels in M1 in which the signal changed above a threshold of Z = 2 during the respective activation intervals relative to rest, for each set (X2-X1, see text) during the two activation intervals of the initial and late sets of the session as well as when a new sequence was introduced is shown. Initial pattern: Averaged data from five subjects from the first two sets of each subject showing the initial ordering effect irrespective of sequence type, lesser extent of M1 activated during the second compared with the first interval. Late pattern: Averaged data from the two late sets in the session (sets 6 and 7) of five subjects showing the reversed ordering effect, irrespective of sequence type, larger extent of M1 activated during the second compared with the first interval. New sequence: Averaged data from three subjects (one set each) performing a new sequence, ordering effect reverted to the naive, initial pattern with smaller extent of M1 activated during the second compared with the first interval. (Bars = SD.) (B and C) Behavioral effects. Speed (B) and accuracy (C) of performance recorded during a test interval of 30 sec for two sequences (one randomly assigned to be trained or other the untrained control) before training (before), after a few minutes of externally paced performance of the designated trained sequence (after), and 24 hr later, with no additional training in the interval. Data from 12 subjects. An ANOVA showed that the effects of training, time and the interaction time*training were significant [F(2,55) = 33.06 P < 0.001, F(1,55) = 26.83 P < 0.001, F(2,55) = 3.57 P < 0.03, respectively, for speed; F(2,55) = 29.58 P < 0.001, F(1,55) = 47.73 P < 0.001, F(2,55) = 6.34 P = 0.003, respectively, for errors].